Background In high-income temperate countries, the number of hospitalizations for heart failure (HF) and acute myocardial infarction (AMI) increases during the winter. This finding has not been fully investigated in low- and middle-income countries with tropical and subtropical climates. We investigated the seasonality of hospitalizations for HF and AMI in Sao Paulo (Brazil), the largest city in Latin America. Methods This was a retrospective study using data for 76,474 hospitalizations for HF and 54,561 hospitalizations for AMI obtained from public hospitals, from January 2008 to April 2015. The average number of hospitalizations for HF and AMI per month during winter was compared to each of the other seasons. The autoregressive integrated moving average (ARIMA) model was used to test the association between temperature and hospitalization rates. Findings The highest average number of hospital admissions for HF and AMI per month occurred during winter, with an increase of up to 30% for HF and 16% for AMI when compared to summer, the season with lowest figures for both diseases (respectively, HF: 996 vs. 767 per month, p<0.001; and AMI: 678 vs. 586 per month, p<0.001). Monthly average temperatures were moderately lower during winter than other seasons and they were not associated with hospitalizations for HF and AMI. Interpretation The winter season was associated with a greater number of hospitalizations for both HF and AMI. This increase was not associated with seasonal oscillations in temperature, which were modest. Our study suggests that the prevention of cardiovascular disease decompensation should be emphasized during winter even in low to middle-income countries with tropical and subtropical climates.

Increased hospitalizations for decompensated heart failure and acute myocardial infarction during mild winters: A seven-year experience in the public health system of the largest city in Latin America

January
Increased hospitalizations for decompensated heart failure and acute myocardial infarction during mild winters: A seven-year experience in the public health system of the largest city in Latin America
Renato Kawahisa Levin 0 1
Marcelo Katz 0 1
Paulo H. N. Saldiva 1
Adriano Caixeta 0 1
Marcelo Franken 0 1
Carolina Pereira 0 1
Salo V. Coslovsky 1
Antonio E. Pesaro 0 1
0 Hospital Israelita Albert Einstein , Sao Paulo, Sao Paulo , Brazil , 2 Instituto de Estudos AvancËados da Universidade de São Paulo , Sao Paulo, Sao Paulo, Brazil, 3 Robert F. Wagner School of Public Service, New York University , New York, New York , United States of America
1 Editor: Eduardo Roque Perna, Instituto de Cardiologia J F Cabral , ARGENTINA
Methods
-
Competing interests: The authors have declared
that no competing interests exist.
Background
In high-income temperate countries, the number of hospitalizations for heart failure (HF)
and acute myocardial infarction (AMI) increases during the winter. This finding has not been
fully investigated in low- and middle-income countries with tropical and subtropical climates.
We investigated the seasonality of hospitalizations for HF and AMI in Sao Paulo (Brazil), the
largest city in Latin America.
Findings
This was a retrospective study using data for 76,474 hospitalizations for HF and 54,561
hospitalizations for AMI obtained from public hospitals, from January 2008 to April 2015.
The average number of hospitalizations for HF and AMI per month during winter was
compared to each of the other seasons. The autoregressive integrated moving average
(ARIMA) model was used to test the association between temperature and hospitalization
rates.
The highest average number of hospital admissions for HF and AMI per month occurred
during winter, with an increase of up to 30% for HF and 16% for AMI when compared to
summer, the season with lowest figures for both diseases (respectively, HF: 996 vs. 767 per
month, p<0.001; and AMI: 678 vs. 586 per month, p<0.001). Monthly average temperatures
were moderately lower during winter than other seasons and they were not associated with
hospitalizations for HF and AMI.
Abbreviations: AMI, acute myocardial infarction;
ARIMA, autoregressive integrated moving average;
HF, heart failure.
Interpretation
The winter season was associated with a greater number of hospitalizations for both HF and
AMI. This increase was not associated with seasonal oscillations in temperature, which
were modest. Our study suggests that the prevention of cardiovascular disease
decompensation should be emphasized during winter even in low to middle-income countries with
tropical and subtropical climates.
Introduction
Coronary artery disease and heart failure (HF) are leading causes of morbidity and mortality
worldwide.[
1
] In low- and middle-income countries, an aging population has been associated
with an increased prevalence of both diseases. In Brazil, HF has become a leading cause of
hospitalization while acute myocardial infarction (AMI) has become the main cause of death.[
2,
3
]
High-income countries with temperate climates are characterized by large seasonal
oscillations in ambient temperature. In these countries, the association between winter and
decompensated cardiovascular diseases has been clearly demonstrated. [
4, 5
] Biological mechanisms
linking low temperatures to higher cardiovascular risk include persistently higher sympathetic
nervous system activation, uncontrolled hypertension, and an increased incidence of
respiratory diseases. Social and environmental mechanisms that hinge not only on low temperatures
but on winter conditions more generallyÐsuch as shorter days, reduced physical activity,
depression, and higher pollution levelsÐmay also explain higher cardiovascular risk.[
6, 7
]
In low- and middle-income countries with a tropical and subtropical climate, the effect of
mild winters on cardiovascular decompensation has not been fully investigated. In these
countries, temperature does not oscillate much across seasons but other social and environmental
factors such as precarious housing conditions, lack of thermal insulation, and greater pollution
might increase the seasonal effect of winter on risk.[8±10]
In our study, we investigated the seasonality of hospitalizations for HF and AMI and tested
the association between monthly average temperatures and hospitalizations for these diseases
in the public health system of Sao Paulo, Brazil, the largest city in Latin America. We
hypothesize that in Sao Paulo, the winter season is associated with increased cardiovascular risk even if
seasonal temperature oscillations remain modest. We also speculate that this association might
be rooted in the socio-economic circumstances faced by our studied population, i.e. the users
of the public health system, such as greater exposure to air pollution, lack of thermal
insulation, precarious housing, and other tribulations faced by those who live with low-income in
such a megacity.
Methods
This was an observational, retrospective study of data obtained from 61 public hospitals in Sao
Paulo. [11] The data was recorded prospectively on a monthly basis from January 2008 to
April 2015 by the National Registry of Public Health, which is maintained by the Brazilian
Public Health System. [12] To record the data, the National Registry requires that hospitals
submit an official form (ªHospital Admission Authorizationº) for each patient that is admitted
under the auspices of the Brazilian Public Health System. This form contains the primary
admission diagnosis and other patient data.
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For our study, the inclusion criteria were: Age >20 years and admission for HF or AMI as
defined by the International Classification of Diseases (ICD-10) [13], in which code I50
represents HF and code I21 represents AMI. Data on monthly average temperatures were obtained
from the Environmental Sanitation Technology Company of Sao Paulo, based on 24 hourly
measurements per day, from six meteorological stations in the city.[14] To calculate monthly
average temperatures for the city, we first calculated average temperatures for each station and
month, and then calculated the mean temperature levels for all stations for each month. This
study was conducted in accordance with The Code of Ethics of the World Medical Association
(Declaration of Helsinki) for experiments involving humans and was approved by the
Institutional Review Board of the Hospital Israelita Albert Einstein. The study was granted a waiver
for informed consent.
Statistical analysis
For each diagnosis, the average number of hospitalizations per month was compared across
the four seasonsÐboth for all patients and within separate gender and ten-year age groupsÐ
using generalized linear models with Poisson distribution, identity link function and
Bonferroni multiple comparisons. The boundaries of each season followed the meteorological
definition for the South Hemisphere [15], i.e. winter is comprised of June, July and August; spring is
comprised of September, October and November; summer includes December, January and
February, and autumn includes March, April and May. Monthly average temperature levels
(mean ± standard deviation) were compared across the four seasons by analysis of variances
and Bonferroni multiple comparisons. The Box-Jenkins autoregressive integrated moving
average (ARIMA) model was used to test the association between ambient temperature and
the average number of hospitalization per month. [16] The modeling process proceeded in
three steps: first, the temporal effect of the series of cardiovascular events was removed by the
ARIMA model; second, model parameters were chosen according to the autocorrelations and
partial autocorrelations; and finally, the white noise or stationary time series was used to
estimate the coefficients. For each series in the study, a regression parameter was added to test the
influence of model specifications on the significance of obtained results. A p<0.05 was
considered statistically significant. All statistical analyses were performed using SPSS statistical
software version 20.0.
Results
During the study period, the National Registry of Public Health recorded a total of 4,823,761
hospital admissions. Using the inclusion criteria outlined above, we identified 76,474
hospitalizations for HF (49.9% men, 67.7% 60 years) and 54,561 hospitalizations for AMI (63.3%
men, 55.9% 60 years). Monthly average temperature levels and the number of
hospitalizations for HF and AMI per month are illustrated in Figs 1 and 2. Seasonal average temperature
levels were lowest in the winter (mean ± SD of 17.5 ± 1.3ÊC), moderately lower than the
monthly average temperature recorded during the spring, summer and autumn (respectively,
mean ± SD of 20.3 ± 1.4, 23.3 ± 1.2 and 20.7 ± 1.9; p <0.001 for comparison of winter vs. all
other seasons).
The average number of hospital admissions for HF and AMI per month peaked during
winter, with an increase of up to 30% for HF and 16% for AMI, when compared to summer,
which was the season with lowest figures for both diseases (respectively, HF: 996 vs. 767 per
month, p<0.001; and AMI: 678 vs. 586 per month, p<0.001). These findings were not affected
by gender (Tables 1 and 2). When analyzed within age groups, the average number of
admissions for HF per month during winter was higher in patients older than 40, while the
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Fig 1. Monthly average temperature levels and number of hospitalizations per month for heart failure.
equivalent figure for AMI was higher in patients older than 50 (Tables 1 and 2). Using ARIMA
analysis, we find that the average number of hospitalizations for AMI and HF per month
increases during winter months; however, we did not find an association between temperature
levels and hospitalizations (Table 3).
Fig 2. Monthly average temperature levels and number of hospitalizations per month for acute myocardial infarction.
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Discussion
In our analysis of data for Sao Paulo, we find an increase in the average number of
hospitalizations per month for HF and AMI during the winter when compared to each of the other
seasons, and an increase of up to 30 and 16%, respectively, when winter figures are compared to
summer. The monthly average temperature during winter was only moderately lower than in
other seasons, and we did not observe an association between ambient temperature and
hospital admissions.
Numerous studies examining data from high-income countries with temperate climates
have demonstrated an association between winter and the incidence and mortality from HF
and AMI. [17±19] In these countries, the oscillation in temperature levels across seasons is
P<0.001 for comparisons between winter vs. other seasons, and spring vs. other seasons. There was no difference between summer and autumn. AMI, acute
myocardial infarction. AMI, acute myocardial infarction
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Parameter
MA 1.12
Temperature
MA 1.12
Temperature
quite large, with a marked decrease during the winter. Extremely cold temperatures can induce
systemic adrenergic activation, increased peripheral vascular resistance, and systemic
hypertension resulting in increases in both cardiac oxygen consumption and demands on cardiac
output.[20, 21] Low ambient temperatures can also induce the release of fibrinogen and
coagulation factors that may result on a hypercoagulable state and a higher risk of atherothrombosis.
[22]
Similar assessments on the effects of winter on cardiovascular risk in low- and
middleincome tropical countries are scarcer but still suggestive. A study conducted in Havana
(Cuba), found higher mortality in AMI patients during winter.[
8
] In Bangladesh, a study using
one small registry found that hospital admission rates for several cardiovascular
decompensated diseases, including AMI and HF, peaked during the winter.[
9
] Some recent studies have
shown that this increase in cardiovascular risk can be attributed, at least partially, to a decline
in temperature. One large multinational study that tested the association between ambient
temperature and general mortality found that most of the temperature-related deaths could be
attributed to low temperatures typical of winter and not to high temperatures typical of
summer. [23] Even if this association was more evident in high-income temperate countries, it was
still present in low- and middle-income tropical countries such as Brazil and Thailand. Studies
conducted in Taipei and Hong Kong also found that low temperature days and daily
temperature oscillation are associated with increased risk for AMI and HF.[24±26] Similar to Sao
Paulo, Taipei and Hong Kong have a humid subtropical climate and mild winters. Unlike Sao
Paulo, however, they have a slightly wider gap in monthly average temperatures across seasons
[27] and a much higher income per capita. [28] These differences hinder a direct comparison
across these sites but they also suggest that lower temperatures might not be the only variable
affecting the observed association between winter and increased hospitalizations for HF and
AMI.
Two previous studies have examined the influence of winter on cardiovascular risk in Sao
Paulo, Brazil. One study found an increase in mortality for AMI during winter but it relied
exclusively on data for a single year (1997) [29]. Another study examined a larger dataset and
found that hospitalization for HF increases during winter. [30] However, this study did not
test whether this perceived increase was statistically significant and neither did it incorporate
ambient temperature into its analysis.
In our study, we found an increase in hospitalizations for HF and AMI during the winter
despite a moderate average winter temperature of 17.5ÊC, only 2.8 to 5.8ÊC lower than the
other seasons. Besides the direct effects of low ambient temperatures on the cardiovascular
system, environmental aspects linked to winter could help explain our findings. Sao Paulo winters
are characterized by low humidity, limited rains and a higher frequency of thermal inversions,
which occur when cold air gets trapped near the surface and underneath a layer of warmer air.
[31] Together, these conditions prevent the dispersion of pollutants such as carbon monoxide
6 / 10
(CO), nitrogen dioxide (NO2), sulfur dioxide (SO2), and inhalable particulate matter (PM10)
that are associated with increased cardiovascular risk. [32] Lower ambient temperatures, low
humidity, and high pollution could also reinforce each other as they contribute to a higher
incidence of respiratory diseases and influenza, with a consequent increase in cardiovascular
risk.[33]
On the socio-economic side, Sao Paulo is the economic engine of Brazil, with an estimated
11,253,503 inhabitants. [34] The city has been characterized by several decades of mostly
unplanned urban growth. At present, approximately 40% of the population of its larger
metropolitan area live in precarious housing conditions.[35] Moreover, its inhabitants are often
exposed to massive traffic jams and significant pollution. [36] These issues are especially salient
to its low-income citizens, a group that relies heavily on the services provided by the Brazilian
Public Health System. The importance of socio-economic variables on winter risk has been
noted in a recent multicenter study conducted in 14 European countries. This study found
that Portugal had the highest rate of excess winter mortality, even though it has a milder winter
than several other countries included in the analysis. [37] This study also demonstrated that
per capita national income, per capita health expenditure, poverty rates, and several indicators
of residential thermal standards were associated with excess winter mortality. These findings
support the hypothesis that not only temperature levels, but also adverse socio-economic
conditions may increase the effect of winter on cardiovascular risk.
Our study has several limitations. First, this was an observational study and despite
statistical adjustments, a causal and definite relationship between seasonality and hospital admissions
for HF and AMI cannot be determined. Second, we analyzed data maintained by the Brazilian
Public Health System that accounts for 66% of hospital admissions in the country [38]. Data
pertaining to the private health system were not available. Third, our dataset does not contain
information on clinical characteristics besides age and sex. Similarly, we lacked data on
pollution levels. For these reasons, we could neither adjust our results for comorbidities nor explore
the direct effect of pollution on cardiovascular risk during winter. Finally, the Brazilian
National Registry of Public Health provides only monthly data on hospital admissions so we
could not analyze daily or weekly variation that could have revealed an association between
cold days and an increase in cardiovascular risk. In spite of these limitations, our analysis of
data for Sao Paulo demonstrates the seasonality of hospital admissions for HF and AMI, with
an increase during relatively mild winters. Considering that mean temperatures were only
moderately lower during the winter when compared to other seasons, our study raises the
possibility that other factors related to disorderly urban occupation and urban poverty, such as a
greater exposure to pollution and the lack of thermal protection in precarious housing, might
also be associated with the seasonal increase in cardiovascular risk. This broader issue deserves
further investigation.
In conclusion, in the megacity of Sao Paulo, winters were associated with an increased
number of hospitalization for both HF and AMI. This relationship did not hinge on seasonal
temperature oscillations. Our findings suggest that the prevention of cardiovascular disease
decompensation should be emphasized during winter even in low to middle-income countries
with modest temperature oscillations.
Supporting information
S1 Dataset. For hospital admissions for heart failure and acute myocardial infarction.
(XLS)
7 / 10
Acknowledgments
This research received no specific grant from any funding agency in the public, commercial,
or not-for-profit sectors. We would like to acknowledge RogeÂrio Ruscitto Prado for his
support with statistics.
Author Contributions
Investigation: Renato Kawahisa Levin, Paulo H. N. Saldiva, Adriano Caixeta, Carolina Pereira,
Salo V. Coslovsky, Antonio E. Pesaro.
Methodology: Renato Kawahisa Levin, Marcelo Katz, Salo V. Coslovsky, Antonio E. Pesaro.
Project administration: Carolina Pereira, Antonio E. Pesaro.
Supervision: Marcelo Franken, Antonio E. Pesaro.
Writing ± original draft: Renato Kawahisa Levin, Marcelo Katz, Paulo H. N. Saldiva, Adriano
Caixeta, Antonio E. Pesaro.
Writing ± review & editing: Renato Kawahisa Levin, Marcelo Katz, Paulo H. N. Saldiva,
Adriano Caixeta, Marcelo Franken, Carolina Pereira, Salo V. Coslovsky, Antonio E. Pesaro.
8 / 10
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